Seasonal variation of bat-flies (Diptera: Streblidae) in ...

1 downloads 0 Views 317KB Size Report
May 25, 2017 - nología (CONACyT, Red Temática del Código de Barras de la Vida ... Red-billed Choughs: a non-parasitic interaction? J. Avian Biol.

Mammalia 2018; 82(2): 133–143

Valeria B. Salinas-Ramos*, Alejandro Zaldívar-Riverón, Andrea Rebollo-Hernández and L. Gerardo Herrera-M

Seasonal variation of bat-flies (Diptera: Streblidae) in four bat species from a tropical dry forest DOI 10.1515/mammalia-2016-0176 Received December 6, 2016; accepted April 11, 2017; previously published online May 25, 2017

Abstract: Seasonality of climate promotes differences in abundance and species composition of parasites, affecting host-parasite interactions. Studies have reported seasonal variation in bat-flies, which are obligate bat ectoparasites. We characterized the bat-fly load of three insectivores [Pteronotus davyi (Gray), Pteronotus parnellii (Gray) and Pteronotus personatus (Wagner)] and one nectarivorous [Leptonycteris yerbabuenae (Martínez and Villa-R.)] bat species in a tropical dry forest to test the existence of seasonality in response to the availability of resources during the wet and dry seasons. We collected 3710 bat-fly specimens belonging to six species and two genera from 497 bats. Most of the ectoparasite load parameters examined (mean abundance, mean intensity, richness, etc.), including comparisons among reproductive conditions and sex of the host, were similar in both seasons. Prevalence was the parameter that varied the most between seasons. The six bat-fly species were found in all bat species except P. personatus. The latter species and L. yerbabuenae had four and five bat-fly species in the wet and dry seasons, respectively. This study provides significant information of ectoparasites ecology in relation to seasonality, contributes to the understanding of host-parasite relationships in tropical dry forests and discusses the relevance of the *Corresponding author: Valeria B. Salinas-Ramos, Posgrado en Ciencias Biológicas, Instituto de Biología, Universidad Nacional Autónoma de México, A. P. 70-153, Ciudad de México, C. P. 04510, Mexico, e-mail: [email protected] Alejandro Zaldívar-Riverón: Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México, C. P. 04510, Mexico Andrea Rebollo-Hernández: Laboratorio de Acarología, Facultad de Ciencias, Departamento de Biología Comparada, Universidad Nacional Autónoma de México, Ciudad de México, C. P. 04510, Mexico L. Gerardo Herrera-M: Estación de Biología Chamela, Instituto de Biología, Universidad Nacional Autónoma de México, A.P. 21, San Patricio, C. P. 48980, Jalisco, Mexico

abiotic and biotic factors that could impact host-parasite interactions. Keywords: Chiroptera; ectoparasites; Mormoopidae; Phyllostomidae; seasonality; Streblidae.

Introduction Parasite communities are directly or indirectly influenced by both environmental variations (Marcogliese 2001, Tinsley et al. 2011, Pilosof et al. 2012) and by changes in host population attributes (e.g. density; Arneberg et  al. 1998, Beldomenico and Begon 2010). Abiotic factors play an important role in parasite species richness, transmission, intensity of infestation (Moyer et  al. 2002, Mas-Coma et  al. 2008, Gotz et  al. 2010), developmental success, abundance (Hudson et al. 2006, Gotz et al. 2010), prevalence, activity and growth (Merino and Potti 1996, ­Klukowski 2004, Dietsch 2005, Antoniazzi et  al. 2010). This is especially the case of species that do not live permanently on their hosts, where their abundance, intensity and prevalence can be influenced by external factors such as temperature, humidity and precipitation (Marshall 1981, Merino and Potti 1996, Hawlena et  al. 2006, Gray et al. 2009, Postawa and Furman 2014). Bats have a variety of ectoparasites, including mites and ticks (Arachnida: Acari), fleas (Siphonaptera), batbugs (Hemiptera, Cimicidae) and bat-flies (Diptera, Nycteribiidae and Streblidae) (Reisen et al. 1976, Lourenço and Palmeirim 2008, Barrientos 2012). Several studies have reported seasonal variation in ectoparasite load on bats (Reisen et al. 1976, Villegas-Guzman et al. 2005, Lourenço and Palmeirim 2008). These studies have found that reproductive activity of ectoparasites fluctuates seasonally, reproducing more intensively during bat’s pregnancy and nursing seasons, and reducing their reproductive activity during winter (Lourenço and Palmeirim 2008). Bat-flies are obligate ectoparasites of bats and have an indirect transmission cycle (Dick and Patterson 2007). During this cycle, the female deposits its larvae in the

Authenticated | [email protected] author's copy Download Date | 2/27/18 1:24 AM

134      V.B. Salinas-Ramos et al.: Seasonal variation of bat-flies bat’s roost, then the larvae immediately pupate and undergo metamorphosis and subsequently the enclosed flies locate an appropriate host (Dick and Patterson 2007). As these dipteran ectoparasites are exposed to the climatic conditions during their life cycle, their abundance might be particularly affected by the environmental conditions as for other ectoparasites such as mites, ticks and fleas (Merino and Potti 1996, Gray et al. 2009). Variation in bat-fly abundance might be attributable to the effect of climate on the flies or on their hosts (Villegas-Guzman et  al. 2005, Pilosof et  al. 2012). In some bat-fly species, warmer ambient temperatures appear to favor bat-fly abundance and development (Pilosof et al. 2012), whereas in others their frequency of occurrence is higher during winter (Villegas-Guzman et al. 2005). Few studies have described the effect of environmental conditions on host-parasite interactions, being mostly based on endoparasites and/or aquatic environments (Valtonen et al. 2003, King et al. 2007). It has been reported that climate seasonality not only affects abundance and richness of ectoparasites, but may also impact host availability and thus parasite prevalence (Lareschi and Krasnov 2010, Lumbad et  al. 2011, Fagir et  al. 2015, Mysterud et  al. 2016). Knowledge of the effects of environmental conditions on ectoparasites is relevant as they have an important selective pressure on the evolution, fitness and population dynamics of their hosts (Lehmann 1993, Stanko et  al. 2006), and consequently on community structure (Mouritsen and Poulin 2002). Moreover, the magnitude of parasites impact on ecosystems may not be fully understood unless weather-mediated host-parasite interactions are considered (Mouritsen and Poulin 2002). In this work, we investigate the existence of seasonality of parasite load of bat-fly (Diptera: Streblidae) populations and communities on three mormoopid insectivorous [Pteronotus davyi (Gray), Pteronotus parnellii (Gray) and Pteronotus personatus (Wagner)] and one phyllostomid nectarivorous [Leptonycteris yerbabuenae (Martínez and Villa-R.)] bat species. These species roost within a cave in a small island (Don Panchito Island) located near the Mexican Pacific coast in the Chamela region (Stoner et al. 2003). These bat species have a tropical distribution; nevertheless Chamela region is highly seasonal, making it a suitable model to study seasonality. This region is mainly composed of seasonal tropical dry forest, with most of the rainfall occurring from June to November (Bullock 1995, Pringle et al. 2012, Méndez-Alonzo et al. 2013). Tropical dry forests have extreme changes in the physiognomy and available resources during wet and dry seasons, thus altering the composition and diversity of fauna (Palacios-Vargas et  al. 2007). In particular, the

abundance of arthropods in tropical locations reaches its highest level during the wet season (Levings and Windsor 1982), a pattern that has been previously reported for Chamela (Pescador-Rubio et  al. 2002). The cave in Don Panchito Island has a higher bat density during the wet season (Ceballos et al. 1997, Stoner et al. 2003), when food resources are more abundant in the region (Ceballos et al. 1997, Pescador-Rubio et al. 2002). Accordingly, we predict that bat-flies load will exhibit seasonal changes in abundance and diversity, with the highest values during the wet season, when the resources are higher in the area (Ceballos et al. 1997, Pescador-Rubio et al. 2002).

Materials and methods Study area Don Panchito Island is located off the Mexican Pacific coast of Chamela, Jalisco (19.5350 N, 105.08832 W). The region is mainly composed of tropical dry forest, with a mean annual temperature of 24.9°C (Rzedowski 1981, Bullock 1995) and 85% of the ~750 mm of yearly rain from July to November (Bullock 1995, Pringle et al. 2012, Méndez-Alonzo et al. 2013). Vegetation in the island mainly consists of tropical deciduous and tropical semi-deciduous forests (Rzedowski 1981). This island has a cave that serves as daytime roost for Leptonycteris yerbabuenae, Pteronotus davyi, Pteronotus parnellii, Pteronotus personatus and Mormoops megalophyla (Peters), though the last species was rarely encountered and therefore was not considered for this study. We collected bat ectoparasites during the dry (June 2012, April 2013 and May 2014) and the wet (November 2012, July 2013, November 2013 and September 2014) seasons. Adult bats were trapped with sweep nets inside the cave during the morning (before 9 am), and then were placed in individual cotton bags and transported to the Chamela Biological Station owned by the Institute of Biology, National Autonomous University of Mexico (IB UNAM). The body (back, tail, wings, ears, uropatagium, etc.) of all bats and the bag where they were kept were subsequently examined for streblids, which were sorted out and preserved in 95% ethanol.

Ectoparasite identification All bat-fly specimens were examined with a Leica® ES2 (Wetzlar, Germany) stereomicroscope and identified to species level using the relevant taxonomic keys Authenticated | [email protected] author's copy Download Date | 2/27/18 1:24 AM

V.B. Salinas-Ramos et al.: Seasonal variation of bat-flies      135

(Wenzel  et  al. 1966, Jirón-Porras and Fallas-Barrantes 1974, Wenzel 1976, Guerrero 1993). Misidentification of species can have profound consequences in ecological studies, which could derive in an error cascade effect (Bortolus 2008, Vink et  al. 2012). At this respect, the simultaneous use of morphology-based taxonomy and DNA sequence data can help to improve delimitation of species and identification accuracy (Dexter et al. 2010). We therefore molecularly confirmed the species boundaries among the bat-fly species identified by morphology generating sequences of a fragment belonging to the DNA barcoding locus [cytochrome oxidase I (COI) mitochondrial DNA gene; Hebert et al. 2003a,b]. Genomic DNA was extracted from two to five specimens assigned to each identified bat-flies species, placing each individual in 50 μl of 5% (w/v) Chelex (Bio-Rad, Hercules, CA, USA) with 12 mg/ml of proteinase K, followed by digestion at 55°C for 2 h. Proteinase K was subsequently heat-inactivated at 96°C for 15 min. Samples were vortexed for 10–15 s and the Chelex was pelleted by centrifugation at 13,000 g for 30 s. The COI fragment was amplified using the LCO1460/HCO2198 primers (Folmer et  al. 1994) and the conditions described by Ceccarelli et al. (2012). Unpurified PCR products were sent for sequencing to the IB UNAM. Sequences were edited with the program four peaks version 1.8 (http://nucleobytes.com/4peaks/) and aligned manually based on their translated amino acids. Corrected COI divergences were obtained using K2P distance model (Kimura 1980) and visualized building a neighbor-joining (NJ) tree with the program PAUP version 4.0a147 (Swofford 2003). We followed the Barcode Index Number (BIN) system (2% genetic divergence criterion) to delimit “barcoding species”, which represents a practical, generally reliable approach to delimit animal species, including insects (Hebert et al. 2003a,b, Ratnasingham and Hebert 2013). The COI sequences generated in this study can be retrieved from GenBank (accession nos KY882237-62).

Statistical analyses We first characterized the seasonal variation in ectoparasite load with the following descriptors of parasite populations: prevalence, mean abundance and intensity during the dry and wet seasons. A χ2-test with the prevalence data and a bootstrap test with the mean abundance and intensity values of each bat-fly species were performed to evaluate for significant differences between seasons. The proportion of infested hosts, the average number of total bat-flies per host individual examined, and the average

number of total bat-fly species per infested host individual were also calculated for the three insectivorous bat species considering the total bat-fly species records. These values were compared between the following pair combination of host reproductive conditions and sexes during wet and dry seasons with the χ2 and bootstrap tests to assess for statistical differences in ectoparasite loads: (1) lactating, pregnant and inactive females and (2) inactive females and males. We did not capture any reproductive bat male during both seasons. The above analyses were conducted with the program Quantitative Parasitology version, 3.0 (Reiczigel and Rózsa 2005), using a significance level of p ≤ 0.05. We did not consider Leptonycteris yerbabuenae because most of the individuals collected were males. Richness, Shannon-Wiener and Gini-Simpson indexes were calculated to assess the diversity of ectoparasite species during both seasons for each bat species. We transformed indexes values to the effective number of species (MacArthur 1965, Hill 1973) to unify an intuitive interpretation of diversity (Jost 2006). Graphics and descriptive analyses were conducted with the program GraphPad prism version 6.0 (GraphPad Software, Inc., La Jolla, CA, USA).

Results Bat-fly species identification We collected 497 bats and 3710 bat-flies specimens that were morphologically assigned to six streblid species belonging to the genera Trichobius and Nycterophilia (Table 1). A NJ phenogram showing the corrected COI distances among the sequenced specimens is showed in Figure 1. The DNA sequence-based species delimitation was congruent with five of the six species identified by morphology. The intra and interspecific corrected genetic distances among the aforementioned five species varied from 0 to 0.95% and from 2.85 to 17.56%, respectively. Sequences of three individuals were generated for Nycterophilia parnelli, of which the two obtained from Pteronotus parnelli had considerably high pairwise distances with the specimen collected from Leptonycteris yerbabuenae (3.02 and 3.5%). We could not find any consistent morphological difference among these specimens and thus regarded them as a single putative species. Except for Pteronotus personatus, in which Trichobius yunkeri was absent, the six bat-flies species were shared by all bat species (Table 1). Fly species were found during both seasons in most bat species except in two Authenticated | [email protected] author's copy Download Date | 2/27/18 1:24 AM

136      V.B. Salinas-Ramos et al.: Seasonal variation of bat-flies Table 1: Frequencies of bat-flies species captured from four bat species during the dry and wet seasons. Leptonycteris  yerbabuenae 

   

Pteronotus davyi   

Pteronotus parnellii   

Pteronotus personatus

Dry 

Wet

Dry 

Wet

Dry 

Wet

Dry 

Wet

Bats captured/% of infested  Total fly species  

18/100  212 

139/68  401 

60/81  434 

53/71  112 

42/88  269 

117/88  2907 

18/89  67 

43/67 118

Streblid species  Nycterophilia coxata  Nycterophilia fairchildi  Nycterophilia parnelli  Trichobius sphaeronotus  Trichobius johnsonae  Trichobius yunkeri

Frequencies of bat-flies/% of bat-flies 78/37  157/39  31/7  8/4  22/5  83/19  4/2  13/3  6/1  116/55  90/22  149/34  6/3  88/22  160/37  0/0  31/7  5/1 

16/14  63/56  8/7  13/12  21/19  1/0 

39/14  4/1  26/10  69/26  95/35  36/13 

75/3  57/3  150/7  144/7  1116/53  555/26 

16/24  40/60  4/6  2/3  5/7  0 

5/4 105/89 4/3 0 4/3 0

             

Figure 1: Neighbor-joining tree showing the corrected COI distances among specimens of the bat-fly species identified in this study. Names in parentheses indicate bat host species.

cases. Trichobius yunkeri and Trichobius sphaeronotus were found in Leptonycteris yerbabuenae and P. personatus only during the wet and dry seasons, respectively. The percentage of infected individuals of L. yerbabuenae, Pteronotus davyi and P. personatus were higher during the dry

season, whereas for Pteronotus parnellii this percentage was the same in both seasons (80%; Table 1). The prevalence, mean abundance and intensity of each bat-fly species are shown in Table 2. Most parameter values were similar in the wet and dry seasons except in Authenticated | [email protected] author's copy Download Date | 2/27/18 1:24 AM

32 (23.30–40.9)  25 (17.30–33.60)  46 (36.90–55.60)  39 (30.40–48.80)  74 (65.50–82.00)  45 (36.10–54.80)  5 (0.60–15.80)  56 (39.90–70.90)  7 (1.50–19.10)  0  7 (1.50–19.10)  0.00 

33 (13.30–59.00)  61 (35.7–82.70)  17 (3.60–41.40)  11 (1.40–34.70)  28 (9.70–53.50)  0.00 

19 (89.40–32.0)  53 (38.6–66.7)  9 (3.10–20.70)  13 (5.50–25.30)  19 (9.40–32.00)  2 (0.00–0.10) 

18 (9.50–30.40)  48 (35.20–61.60)  7 (1.80–16.20)  40 (27.60–53.50)  65 (51.6–76.9)  7 (1.8–16.20) 

31 (17.60–47.10)  9 (2.70–22.60)  36 (21.60–52.00)  24 (12.10–39.50)  59 (43.30–74.40)  45 (29.80–61.30) 

52 (43.20–60.30)  11 (6.20–17.20)  7 (3.50–12.80)  31 (23.40–39.30)  16 (10.20–23.00)  6 (3.00–11.90) 

94 (72.70–99.90)  17 (3.60–41.4)  6 (0.10–27.30)  83 (58.60–96.40)  17 (3.60–41.40)  0 

Dry 

0.00  0.63  0.26  0.02  0.02  0.00 

0.93  0.03  0.24  0.07  0.07  0.99 

0.94  0.63  0.58  0.00  0.00  0.21 

0.00  0.46  0.79  0.00  0.92  0.00 

Prevalence (%; 95% CI)    Wet  p-Value

0.88 (0.27–2.56)  2.22 (1.17–3.89)  0.22 (0.00–0.50)  0.11 (0.00–0.22)  0.27 (0.05–0.44)  0.00 

0.92 (0.44–1.76)  0.09 (0.02–0.19)  0.61 (0.35–1.02)  1.64 (0.59–3.86)  2.26 (1.24–4.94)  0.85 (0.5–1.38) 

0.51 (0.21–1.27)  1.38 (0.86–2.34)  0.10 (0.01–0.23)  2.48 (1.43–4.32)  2.66 (1.80–4.12)  0.08 (0.01–0.18) 

4.33 (2.98–6.00)  0.44 (0.00–1.22)  0.22 (0.00–0.66)  6.44 (3.33–11.11)  0.33 (0.00–0.66)  0.00 

Dry 

0.11 (0.00–0.34)  2.44 (1.44–4.37)  0.09 (0.00–0.23)  0.00  0.09 (0.00–0.23)  0.00 

0.64 (0.44–0.92)  0.48 (0.30–0.75)  1.28 (0.93–1.85)  1.23 (0.87–1.76)  9.54 (7.14–12.7)  4.74 (3.03–8.05) 

0.30 (0.13–0.63)  1.18 (0.75–2.17)  0.15 (0.03–0.34)  0.24 (0.09–0.52)  0.39 (0.13–1.18)  0.01 (0.00–0.05) 

1.12 (0.85–1.48)  0.15 (0.08–0.26)  0.09 (0.03–0.17)  0.64 (0.45–0.94)  0.63 (0.28–1.89)  0.22 (0.08–0.48) 

0.31  0.82  0.37  0.14  0.14  0.00 

0.27  0.00  0.01  0.59  0.00  0.02 

0.43  0.68  0.56  0.02  0.00  0.18 

0.08  0.00  0.60  0.02  0.43  0.09 

Mean abundance (95% CI)    Wet  p-Value

2.66 (1.17–5.50)  3.63 (2.18–5.73)  1.33 (1.00–1.67)  1.00 (0.00)  1.00 (0.00)  0.00 

3.00 (1.85–5.08)  1.00 (0.00)  1.73 (1.27–2.40)  6.90 (3.50–14.50)  3.80 (2.28–9.38)  1.89 (1.37–2.74) 

2.81 (1.64–5.82)  2.86 (2.00–4.52)  1.50 (1.00–1.75)  6.20 (3.88–10.10)  4.10 (2.95–6.15)  1.25 (1.00–1.50) 

4.58 (3.22–6.29)  2.66 (1.00–3.67)  4.00 (0.00)  7.73 (4.28–12.50)  2.00 (0.00)  0.00 

Dry 

2.50 (2.00–2.50)  4.38 (2.96–7.47)  1.33 (1.00–1.67)  0.00  1.33 (1.00–1.67)  0.00 

2.02 (1.57–2.62)  1.96 (1.48–2.69)  2.77 (2.13–3.70)  3.13 (2.48–4.30)  12.82 (9.93–16.7)  10.88 (7.02–17–40) 

1.60 (1.00–2.60)  2.25 (1.54–3.65)  1.60 (1.00–2.20)  1.85 (1.14–2.86)  2.10 (1.00–5.10)  1.00 (0.00) 

2.18 (1.75–2.81)  1.46 (1.13–1.80)  1.30 (1.00–1.80)  2.09 (1.60–2.75)  4.00 (2.09–11.50)  3.44 (1.89–5.78) 

Wet 

0.88 0.60 1.00 1.00 0.55 0.00

0.53 0.02 0.03 0.22 0.00 0.02

0.34 0.45 0.81 0.03 0.14 1.00

1.00 0.00 1.00 0.03 0.41 1.00

p-Value

Mean intensity (95% CI)

p-Values correspond to comparison between seasons of prevalence with χ2-test and to comparisons of abundance and intensity with bootstrap test. Confidence intervals (CI) were set in 95% of probability.

Leptonycteris yerbabuenae  Nycterophilia coxata    Nycterophilia fairchildi    Nycterophilia parnelli    Trichobius sphaeronotus   Trichobius johnsonae    Trichobius yunkeri   Pteronotus davyi  N. coxata    N. fairchildi    N. parnelli    T. sphaeronotus    T. johnsonae    T. yunkeri   Pteronotus parnellii  N. coxata    N. fairchildi    N. parnelli    T. sphaeronotus    T. johnsonae    T. yunkeri   Pteronotus personatus  N. coxata    N. fairchildi    N. parnelli    T. sphaeronotus    T. johnsonae    T. yunkeri  

   

Table 2: Prevalence, mean abundance and intensity of bat-flies species found in the four bat species examined during dry and wet seasons.

V.B. Salinas-Ramos et al.: Seasonal variation of bat-flies      137

Authenticated | [email protected] author's copy Download Date | 2/27/18 1:24 AM

138      V.B. Salinas-Ramos et al.: Seasonal variation of bat-flies the following cases: (1) the prevalence of Nycterophilia coxata, Trichobius sphaeronotus as well as the mean abundance and intensity of Nycterophilia fairchildi and T. sphaeronotus were significantly higher during the dry season in Leptonycteris yerbabuenae; (2) the prevalence and abundance of T. sphaeronotus and Trichobius johnsonae and the intensity of T. sphaeronotus were significantly higher in the dry season in Pteronotus davyi; (3) the prevalence, mean abundance and intensity of N. fairchildi and the mean abundance and intensity of Nycterophilia parnelli, T. johnsonae and Trichobius yunkeri were significantly higher in the wet season in Pteronotus parnellii; and (4) the prevalence of N. coxata, T. sphaeronotus and T. johnsonae were significantly higher during the dry season in Pteronotus personatus. In most cases, the percentage of infested bats and the average number of bat-flies per examined and infested host individual did not differ between seasons and between reproductive conditions and sexes (Table 3). However, in Pteronotus davyi the average number of parasites per examined and infested host in inactive females was significantly higher during the dry than in the wet season. The average number of parasites per infested host was also significantly higher in inactive males than in inactive females in the wet season in P. davyi, whereas the average number of parasites per examined and infested host was significantly higher in lactating than pregnant females, as well as in lactating than inactive females in the wet season in Pteronotus parnellii. In addition, the average number of parasites per infested host was significantly higher in inactive males than inactive females in the wet season in Pteronotus personatus (Table 3). Ectoparasite richness was identical in both seasons in Pteronotus davyi and Pteronotus parnellii (n = 6). Leptonycteris yerbabuenae had one less bat-fly species (n = 5) in the dry season, whereas Pteronotus personatus had the lowest number of bat-fly species during the wet season (n = 4) (Figure 2). In terms of diversity, the effective number of species was higher in L. yerbabuenae, P. davyi and P. parnellii during the wet season, whereas in P. personatus it was higher in the dry season (Figure 3).

Discussion and conclusion Seasonal variation in bat-fly load We characterized the ectoparasite load of four bat species to explore the presence of seasonal changes in the descriptors of parasite populations and diversity in response to

ambient fluctuations, which impact the resources of the area and the density of the hosts. Our hypothesis of seasonality in ectoparasite load was rejected in most of the examined host-parasite parameters. Our prediction of higher ectoparasite load during the wet season was only supported in Pteronotus parnellii by higher mean abundance and intensity of four bat-fly species, as well as by a higher prevalence in one bat-fly species. However, we also found a higher prevalence, mean abundance and intensity of some bat-fly species during the dry season for the remaining three bat species examined. Our results support the contention that some of the bat-fly species associated with Pteronotus parnellii are favored indirectly by the environmental conditions that occur during the wet season, may be with the density of this host. Consistent variations in population abundance are found among communities of parasites (Arneberg et al. 1998). Epidemiological theory indicates that several characters of host species may affect the density of ectoparasite populations (Anderson and May 1978, May and Anderson 1978, Arneberg et  al. 1998). For directly transmitted parasites, host population density could increase the probability of parasite transmission due to contact with its host (Arneberg et  al. 1998, Stanko et  al. 2006). In Don Panchito Island, the density of P. parnellii is higher from the end of the dry (end of June) to the beginning of the wet season (August) (Stoner et al. 2003). Moreover, it has been reported that in July and August the majority of bats in the cave are individuals of P. parnellii (Stoner et al. 2003). This variation in the density might explain the higher abundance and intensity of four bat-fly species in P. parnellii during the wet season. The higher values obtained for some of the ectoparasite load parameters during the dry season in the remaining bat species agree with a previous study that found that ectoparasite species of non-volant mammals had higher prevalence and mean intensity of infestation in the dry season, when the food resources are lower (Sponchiado et al. 2015). Similar to Stoner et al. (2003), we noticed that Don Panchito’s cave has a higher bat density during the wet season, when food resources are more abundant in the region (Ceballos et al. 1997, Pescador-Rubio et al. 2002). If bat density increases during the wet season, host availability for ectoparasites is also higher and they might have the possibility to select the most suitable hosts (Blanco et  al. 1997, Dawson and Bortolotti 1997). On the other hand, in the dry season, when the females of Leptonycteris yerbabunae migrate to Sonora-Arizona desert and the density of bats is lower, host availability for ectoparasites is limited and they might try to parasitize any host individual that is available. This might explain why some Authenticated | [email protected] author's copy Download Date | 2/27/18 1:24 AM



n  83.3 (0.58–0.96)/86.4 (0.65–0.97)  83.3 (0.58–0.96)/85.7 (0.57–0.98)  83.3 (0.58–0.96)/78.6 (0.59–0.91)  64.5 (0.45–0.80)/86.4 (0.65–0.97)  94.7 (0.85–0.98)/92.9 (0.66–0.99)  94.1 (0.71–0.99)/64.7 (0.38–0.85)  72.7 (0.39–0.94)/88.1 (0.74–0.96)  94.7 (0.85–0.98)/88.1 (0.74–0.96)  72.7 (0.39–0.94)/92.9 (0.66–0.99)  72.7 (0.39–0.94)/94.1 (0.71–0.99)  88.1 (0.74–0.96)/64.7 (0.38–0.85)  88.3 (0.35–0.99)/100 (0.39–1.00)  88.3 (0.35–0.99)/53.8 (0.25–0.80)  53.8 (0.25–0.80)/100 (0.39–1.00)  70.8 (0.48–0.87)/84.6 (0.54–0.98)  53.8 (0.25–0.80)/70.8 (0.48–0.87) 

54/13  16/11  8/37  54/37  8/13  8/16  37/11 

5/4  5/7  7/4  17/11  7/17 

PHI (%) 

15/19  15/12  15/22  20/19 

Inf 

1.00  0.33  0.23  0.44  0.47 

1.00  0.08  0.34  0.27  0.28  0.26  0.06 

1.00  1.00  1.00  0.11 

p-Value 

7.6 (2.8–17.0)/6.5 (3.0–8.25)  7.6 (2.8–17.0)/1.6 (0.69–3.69)  1.6 (0.69–3.69)/6.5 (3.0–8.25)  2.0 (1.25–3.29)/2.5 (1.46–4.23)  1.6 (0.69–3.69)/2.0 (1.25–3.29) 

27.4 (19.6–38.9)/4.0 (2.3–7.2)  7.4 (4.41–12.2)/5.0 (2.17–9.88)  7.73 (2.6–20.4)/10.6 (6.62–18.3)  27.4 (19.6–38.9)/10.6 (6.62–18.3)  7.7 (2.6–20.4)/4.0 (2.3–7.2)  7.7 (2.6–20.4)/7.4 (4.41–12.2)  10.6 (6.62–18.3)/5.0 (2.17–9.88) 

7.8 (4.89–13.5)/1.5 (1.14–1.86)  7.8 (4.89–13.5)/3.7 (2.4–5.1)  7.8 (4.89–13.5)/8.5 (5.43–13.5)  2.8 (1.68–4.59)/1.5 (1.14–1.86) 

THE 

0.79  0.27  0.12  0.60  0.00 

0.00  0.38  0.57  0.00  0.45  0.95  0.10 

0.03  0.10  0.81  0.10 

p-Value 

9.2 (3.8–18.6)/6.50 (3.0–8.25)  9.2 (3.8–18.6)/3.1 (1.57–6.14)  3.1 (1.57–6.14)/6.5 (3.0–8.25)  2.9 (1.95–4.35)/3.0 (1.82–4.82)  3.1 (1.57–6.14)/2.9 (1.95–4.35) 

28.8 (21.1–41.7)/4.3 (2.6–7.9)  7.9 (4.81–13.4) /7.7 (3.5–13.7)  10.6 (4.0–26.1)/12.1 (7.52–20.2)  28.8 (21.1–41.7)/12.1 (7.52–20.2)  0.6 (4.0–26.1)/4.3 (2.6–7.9)  10.6 (4.0–26.1)/7.9 (4.81–13.4)  12.1 (7.52–20.2)/7.73 (3.5–13.7) 

9.4 (6.0–15.6)/1.7 (1.42–2.05)  9.4 (6.0–15.6)/4.4 (3.0–5.5)  9.4 (6.0–15.6)/10.8 (7.27–16.4)  4.40 (3–6.58)/1.7 (1.42–2.05) 

THI 

0.58 0.32 0.19 0.95 0.87

0.00 0.95 0.81 0.00 0.37 0.66 0.27

0.03 0.09 0.66 0.03

p-Value

n, Number of bats collected; Inf, infected; PHI, proportion of hosts infected considering the total bat-flies records; THE, average number of total bat-flies per host individual examined; THI, average number of total bat-flies per infected host individuals; DIF, dry season inactive females; WIF, wet season inactive females; DIM, dry season inactive males; WIM, wet season inactive males; WLF, wet season lactating females; DPF, dry season pregnant females. p-Values correspond to comparisons of PHI with χ 2-test and to comparisons of THE and THI with bootstrap test. Confidence intervals (CI) were set in 95% of probability.

Pteronotus davyi  DIF vs. WIF   18/22   DIF vs. DPF   18/14   DIF vs. DIM   18/28   WIM vs. WIF   31/22  Pteronotus parnellii  WLF vs. DPF   57/14   DIM vs. WIM   17/17   DIF vs. WIF   11/42   WLF vs. WIF   57/42   DIF vs. DPF   11/14   DIF vs. DIM   11/17   WIF vs. WIM   42/17  Pteronotus personatus  WLF vs. DPF   6/4   WLF vs. WIF   6/13   WIF vs. DPF   13/4   WIM vs. DIM   24/13   WIF vs. WIM   13/24 

Species

Table 3: Comparative of bat-flies load in bat individuals of different reproductive conditions in the dry and wet season in three species of bats.

V.B. Salinas-Ramos et al.: Seasonal variation of bat-flies      139

Authenticated | [email protected] author's copy Download Date | 2/27/18 1:24 AM

140      V.B. Salinas-Ramos et al.: Seasonal variation of bat-flies

10

Number of species

Dry

Wet

8 6 4 2 0

L. yerbabuenae

P. davyi P. personatus Bat species

P. parnellii

Figure 2: Richness of bat-flies species registered in four bat species during the dry and wet seasons.

5

Dry

Effective number of species (shannon-wiener index)

4.49 3.85 3.92

4

3.05

3

2

1

1.63 1.10 0.21

0

Wet

L. yerbabuenae

P. davyi

P. personatus

0.27

P. parnellii

Bat species

Figure 3: Effective number of bat-flies species from Shannon-­ Wiener index in four species of bats during the dry and wet seasons.

of the bat-fly species reported higher prevalence, mean abundance and intensity during the dry season in L. yerbabuenae, Pteronotus davyi and Pteronotus personatus. Some other factors that are not associated with the host abundance might affect the seasonal variation of ectoparasites species. For example, Sponchiado et  al. (2015) observed a reduction in infestation level in some mammals when the abundance of ectoparasites increases. They suggested that factor independent of the host abundance might affect the seasonality of some ectoparasites species.

number of bat-flies per examined and infested host did not differ between seasons with some exceptions. These two parameters were significantly higher in lactating than in pregnant and inactive females in Pteronotus parnelli, whereas in the remaining Pteronotus species we did not find differences in these parameters. Thus, lactating condition could influence ectoparasite load during the wet season in P. parnellii. Some parasites synchronize their reproduction and/or activity with that of their host (Price 1980, Marshall 1981, Blanco and Frías 2001, Lourenço and Palmeirim 2008), evolving the ability to detect variations in their host populations to increase their reproductive rates (Sponchiado et  al. 2015). Moreover, a high density of bats in nursing colonies increases the opportunities for their parasites to infest horizontally after reproducing (Christe et al. 2000). We found a higher average number of parasites per examined and infested host in inactive females during the dry than the wet season in Pteronotus davyi. This could be also related to the low density of bats during the dry season, as mentioned above. The ectoparasites thus could parasite any host individual that is available in the dry season, whereas in the wet season they could select the most suitable host. We did not find a pattern in the ectoparasite load between inactive females and males for the examined bat species. However, the average number of parasites per infested and examined host was higher in inactive males than in females during the wet season in Pteronotus davyi and Pteronotus personatus, respectively. The intensity and number of parasites are usually higher in juveniles and females than in subadults and males (Chilton et al. 2000, Zahn and Rupp 2004, Lučan 2006, Lourenço and Palmeirim 2008), though authors report that sex is not related to parasite load (Moura et  al. 2003, Miller 2014). Some studies have also shown that males harbor more ectoparasites than female bats (Hart and Pryor 1992, Komeno and Linhares 1999, Zhang et al. 2010). Further studies are needed to investigate other variables that could influence the average number of parasites per infested and examined host in inactive males of P. davyi and P. personatus during the wet season.

Relation between sex, female reproductive condition and bat-fly load

Richness and diversity

The percentage of infested bats considering all the ectoparasites per bat species did not differ significantly in any pair combination of host reproductive conditions and sexes between seasons. In general, the average

Our hypothesis of seasonal changes in ectoparasites richness and diversity is partially supported. Species richness was almost the same in both seasons for the four bat species. We did not find a seasonal pattern in the effective Authenticated | [email protected] author's copy Download Date | 2/27/18 1:24 AM

V.B. Salinas-Ramos et al.: Seasonal variation of bat-flies      141

number of bat-fly species. This value was higher in the wet season in Leptonycteris yerbabuenae, Pteronotus davyi and Pteronotus parnellii, whereas it was higher during the dry season in Pteronotus personatus. Our results contrast with a recent study carried out in the Chamela region, which reported lower bat-flies richness during the wet season (Zarazúa-Carbajal et  al. 2016), where only one (Trichobius sphaeronotus) and four (Trichobius sparsus, Trichobius yunkeri, Trichobius caecus and Nycterophilia parnelli) bat-fly species were found in Leptonycteris yerbabuenae and Pteronotus parnellii, respectively. These authors also suggested that bat-fly species composition was affected by seasonality as a consequence of changes in the abundance of their host. However, the differences found between our and the latter study might be explained by the community composition. The authors collected 246 streblids belonging to 24 species from 145 individuals representing 12 species of bats (Phyllostomidae, Mormoopidae and Noctilionidae) with mist nets. In contrast, we studied a colony of bats that share roost year-round, they were collected inside the cave with sweep nets and our sample was considerably higher (3710 streblids from 497 bats). This study provides significant information of ectoparasites ecology in relation to seasonality, contributes to the understanding of host-parasites relationship in tropical dry forests and remarks the relevance of the abiotic and biotic factors that could impact host-parasite interactions. Parasite species seem to be less specific when ecological barriers to dispersal are removed on experimental conditions (Dick et  al. 2007). We found that sympatric bat species shared most of the bat-fly species, even when not all bat species were phylogenetically closely related. These results suggest that, in some specific cases, the parasites are less specific than that we thought. In some cases, the prevalence, mean abundance and intensity were different during the dry and wet season. We also found that host density might be an important factor driving ectoparasitic infestation. Further studies should explore additional factors that could influence the parasite-host interactions as well as the intensity and prevalence of macroparasites (e.g. microclime, self-grooming, bat age, body condition, bat hormones, immune system, specialization; McLean and Speakman 1997, Christe et  al. 2000, Lourenço and Palmeirim 2008, Luguterah and Lawer 2015, TlapayaRomero et  al. 2015, Rivera-García et  al. 2016, Warburton et al. 2016). Acknowledgments: We thank A. Cuxim-Koyoc for his help with bat-fly identification, S. Sánchez-Montes for his suggestions with the statistical analyses and E. Samacá-Sáez

for his help in the laboratory. VBSR was supported by a scholarship given by CONACyT as part of the Programa de Doctorado en Ciencias Biológicas, Universidad Nacional Autónoma de México. Financial support was provided by grants given by the Consejo Nacional de Ciencia y Tecnología (CONACyT, Red Temática del Código de Barras de la Vida, 2013–2015) to V. León-Règagnon and AZR, grants given by CONACyT (proyecto Ciencia Básica 2014  no. 220454) and Dirección General de Asuntos del Personal Académico (DGAPA-UNAM; no. IN207016) to AZR and a grant given by DGAPA-UNAM (no. IN202113) to LGHM. We thank the Programa de Posgrado en Ciencias Biológicas, Instituto de Biología (IB-UNAM) and Estación de Biología Chamela, UNAM, for logistical support during the study.

References Anderson, R.M. and R.M. May. 1978. Regulation and stability of host-parasite population interactions I. Regulatory processes. J. Anim. Ecol. 47: 219–247. Antoniazzi, L.R.D., E. Manzoli, D. Rohrmann, M.J. Silvestri and P.M. Beldomenico. 2010. Climate variability affects the impact of parasitic flies on Argentinean forest birds. J. Zool. 283: 126–134. Arneberg P., A. Skorping, B. Grenfell and A.F. Read. 1998. Host densities as determinants of abundance in parasite communities. Proc. R. Soc. London Ser. B 265: 1283–1289. Barrientos, M.A. 2012. Prevalencia y derminación de ectoparásitos en murciélagos (Chiroptera) y Roedres (Rodentia) en dos localidades de la mixteca poblana: Santo Domingo Tonahuixtla y Teotlalco Puebla, México. Master Thesis. pp. 141. Beldomenico, P.M. and M. Begon. 2010. Disease spread, susceptibility and onfection intensity: vicious circles? Trends Ecol. Evol. 25: 21–27. Blanco, G. and O. Frías. 2001. Symbiotic feather mites synchronize dispersal and population growth with host sociality and migratory disposition. Ecography 24: 113–120. Blanco, G., J.L. Tella and J. Potti. 1997. Feather mites on group-living Red-billed Choughs: a non-parasitic interaction? J. Avian Biol. 28: 197–206. Bortolus, A. 2008. Error cascades in the biological science: the unwanted consequences of using bad taxonomy in ecology. Ambio. 37: 114–118. Bullock, S.H. 1995. Plant reproduction in neotropical dry forest. In: (S.H. Bullock, H.A. Mooney and E. Medina, eds.) Seasonally dry tropical forests. Cambridge University Press, Cambridge, UK. pp. 277–303. Ceballos, G., T.H. Fleming, C. Chávez and J. Nassar. 1997. Population dynamics of Leptonycteris curasoae (Chiroptera: Phyllostonidae) in Jalisco, Mexico. J. Mammal. 78: 1220–1230. Ceccarelli, F.S., M.J. Sharkey and A. Zaldívar-Riverón. 2012. Species identification in the taxonomically neglected, highly diverse, Neotropical parasitoid wasp genus Notiospathius (Braconidae: Doryctinae) based on an integrative molecular and morphological approach. Mol. Phylogenet. Evol. 62: 485–495.

Authenticated | [email protected] author's copy Download Date | 2/27/18 1:24 AM

142      V.B. Salinas-Ramos et al.: Seasonal variation of bat-flies Chilton, G., M.J. Vonhofter, B.V. Peterson and N. Wilson. 2000. Ectoparasitic insects of bats in British Columbia, Canada. J. Parasitol. 86: 191–192. Christe, P., R. Arlettaz and P. Vogel. 2000. Variation in intensity of a parasitic mite (Spinturnix myotis) in relation to the reproductive cycle and immunocompetence of its bat host (Myotis myotis). Ecol. Lett. 3: 207–212. Dawson, R.D. and G.R. Bortolotti. 1997. Ecology of parasitism of nestling American Kestrels by Carnus hemapterus (Diptera: Carnidae). Can. J. Zool. 75: 2021–2026. Dexter, K.G., T.D. Pennington and C.W. Cunningham. 2010. Using DNA to assess errors in tropical tree identifications: how often are ecologists wrong and when does it matter? Ecol. Monogr. 80: 267–286. Dick, C.W. and B.D. Patterson. 2007. Against all odds: explaining high host specificity in dispersal-prone parasites. Int. J. Parasitol. 37: 871–876. Dietsch, T.V. 2005. Seasonal variation of infestation by ectoparasitic chigger mite larvae (Acarina: Trombiculidae) on resident and migratory birds in coffee agroecosystems of Chiapas, Mexico. J. Parasitol. 91: 1294–1303. Fagir, D.M., I.G. Horak, E.A. Ueckermann, N.C. Bennett and H. Lutermann. 2015. Ectoparasite diversity in the eastern rock sengis (Elephantulus myurus): the effect of seasonality and host sex. Afr. Zool. 50: 109–117. Folmer, O., M. Black, W. Hoeh, R. Lutz and R. Vrijenhoek. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotech. 3: 294–299. Gotz, F., R. Harf, S. Sommer and S. Matthee. 2010. Effects of precipitation on parasite burden along a natural climatic gradient in southern Africa-implications for possible shifts in infestation patterns due to global changes. Oikos 119: 1029–1039. Gray, J.S., H. Dautel, A. Estrada-Peña, O. Kahl and E. Lindgren. 2009. Effects of climate change in ticks and tick-borne diseases in Europe. Interdiscip. Perspect. Infect Dis. 2009: 593232. Guerrero, R. 1993. Catalogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del Nuevo Mundo. I. Clave para los generos y Nycterophilinae. Acta Biologica Venezuelica 14: 61–75. Hart, B.L. and P.A. Pryor. 1992. Developmental and hair-coat determinants of grooming behavior in goats and sheep. Anim. Behav. 67: 11–19. Hawlena, H., B.R. Krasnov, Z. Abramsky, I.S. Khokhlova, D. Saltz, M. Kam, A. Tamir, and A.A. Degen. 2006. Flea infestation and energy requirements of rodent hosts: are there general rules? Funct. Ecol. 20: 1028–1036. Hebert, P.D.N., A. Cywinska, S.L. Ball and J.R. DeWaard. 2003a. Biological identifications through DNA barcodes. Proc. Biol. Sci. 270: 313–321. Hebert, P.D.N., S. Ratnasingham and J.R. deWaard. 2003b. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc. Biol. Sci. 270: S96–S99. Hill, M. 1973. Diversity and evenness: a unifying notation and its consequences. Ecology 54: 427–432. Hudson, P.J., I.M. Cattadori, B. Boag and A.P. Dobson. 2006. Climate disruption and parasite-host dynamics: patterns and processes associated with warming and the frequency of extreme climatic events. J. Helminthol. 80: 175–182.

Jirón-Porras, L.F. and F. Fallas-Barrantes. 1974. Presence of a new representer of the genus Nycterophilia Ferris, 1916 (Dipera: Streblidae) in Costa Rica. 22: 67–70. Jost, L. 2006. Entropy and diversity. Oikos 113: 363–375. Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 6: 111–120. King, K.C., J.D. McLaughlin, A.D. Gendron, B.D. Pauli, I. Giroux, B. Rondeau, M. Boily, P. Juneau and D.J. Marcogliese. 2007. Impacts of agriculture on the parasite communities of northern leopard frogs (Rana pipiens) in southern Quebec, Canada. Parasitology 134: 2063–2080. Klukowski, M. 2004. Seasonal changes in abundance of hostseeking chiggers (Acari: Trombiculidae) and infestation on fence lizards, Sceloporus undulates. J. Herpetol. 38: 141–144. Komeno, C. and A.X. Linhares. 1999. Batflies parasitic on some phyllostomid bats in southeastern Brazil: parasitism rates and host–parasite relationships. Mem. Inst. Oswaldo Cruz, Rio de Janeiro 94: 151–156. Lareschi, M. and B.R. Krasnov. 2010. Determinants of ectoparasite assemblage structure on rodent hosts from South American marshlands: the effect of host species, locality and season. Med. Vet. Entomol. 24: 284–292. Lehmann, T. 1993. Ectoparasites: direct impact on host fitness. Parasitol. Today 9: 8–13. Levings, S.C and D.M. Windsor. 1982. Seasonal and annual variation in litter arthropod populations. In: (E.G.Leigh, A.S. Rand and D.M. Windsor, eds.) The ecology of a tropical forest. Smithsonian Institution Press, Washington D.C. pp. 355–387. Lourenço, S.I. and J.M. Palmeirim. 2008. Which factors regulate the reproduction of ectoparasites of temperate-zone cave-dwelling bats? Parasitol. Res. 104: 127–134. Lučan, R.K. 2006. Relationships between the parasitic mite Spinturnix andegavinus (Acari: Spinturnicidae) and its bat host, Myotis daubentonii (Chiroptera:Vespertilionidae): seasonal, sex and age-related variation in infestation and possible impact of the parasite on the host condition and roosting behavior. Folia Parasitol. 53: 147–152. Luguterah, A. and E.A. Lawer. 2015. Effect of dietary guild (frugivory and insectivory) and other host characteristics on ectoparasites abundance (mite and nycteribiid) of chiropterans. Folia Parasitol. 62: 1–21. Lumbad, A.S., L.K. Vredevoe and E.N.Taylor. 2011. Season and sex of host affect intensities of ectoparasites in western fence lizards (Sceloporus occidentalis) on the Central Coast of California. Southwest. Nat. 56: 369–377. MacArthur, R.H. 1965. Patterns of species diversity. Biol. Rev. 40: 510–533. Marcogliese, D.J. 2001. Implications of climate change for parasitism of animals in the aquatic environment. Can. J. Zool. 79: 1331–1352. Marshall, A.G. 1981. The ecology of ectoparasitic insects. Academic Press, London. pp. 459. Mas-Coma, S., M.A. Valero and M.D. Bargues. 2008. Effects of climate change on animal and zoonotic helminthiases. In: (S. de la Rocque, G. Hendrickx and S. Morand, eds.) Climate change: impact on the epidemiology and control of animal diseases. Rev. Sci. Tech. Off. Int. Epiz. 27: 443–458.

Authenticated | [email protected] author's copy Download Date | 2/27/18 1:24 AM

V.B. Salinas-Ramos et al.: Seasonal variation of bat-flies      143 May, R.M. and R.M Anderson. 1978. Regulation and stability of hostparasite population interactions II. Destabilizing processes. J. Anim. Ecol. 47: 249–267. McLean, J.A. and J.R. Speakman. 1997. Non-nutritional maternal support in the brown long-eared bat. Anim. Behav 54: 1193–204. Méndez-Alonzo, R., F. Pineda-García, H. Paz, J.A. Rosell and M.E. Olson. 2013. Leaf phenology is associated with soil water availability and xylem traits in tropical dry forest. Trees 27: 745–754. Merino, S. and J. Potti. 1996. Weather dependent effects of nest ectoparasites on their bird hosts. Ecography 19: 107–113. Miller, C. 2014. Host speficity and ectoparasite load of bat flies in Utila, Honduras. Senior Honors Theses. University of New Orleans. pp. 63. Moura, M.O., M.O. Bordignon and G. Graciolli. 2003. Host characteristics do not affect community structure of ectoparasites on the fishing bat Noctilio leporinus (L., 1758) (Mammalia: Chiroptera). Mem. Inst. Oswaldo Cruz, Rio de Janeiro 98: 811–815. Mouritsen, K.N. and R. Poulin. 2002. Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124: 101–117. Moyer, B.R., D.M. Drown and D.H. Clayton. 2002. Low humidity reduces ectoparasite pressure: implications for host life history evolution. Oikos 97: 223–228. Mysterud, A., L. Qviller, E.L. Meisingset and H. Viljugrein. 2016. Parasite load and seasonal migration in red deer. Oecologia. 180: 401–407. Palacios-Vargas, J.G., G. Castaño-Meneses, J.A. Gómez-Anaya, A. Martínez-Yrizar, B.E. Mejía-Recamier and J. Martínez-Sánchez. 2007. Litter and soil arthropods diversity and density in a tropical dry forest ecosystem in Western Mexico. Biodivers. Conserv. 16: 3703–3717. Pescador-Rubio, A., A. Rodriguez-Palafox, F.A. Noguera. 2002. Diversidad y estacionalidad de Arthropoda. In: (F.A. Noguera, R.J.H. Vega, A.A.N. García and A.M. Quesada, eds.) Historia Natural de Chamela. Instituto de Biología, Universidad Nacional Autónoma de México, Mexico. pp. 183–201. Pilosof, S., C.W. Dick, C. Korine, B.D. Patterson and B.R. Krasnov. 2012. Effects of anthropogenic disturbance and climate patterns of bat fly parasitism. PLoS One 7: 1–7. Price, P. 1980. Evolutionary biology of parasites. Princeton University Press, Princeton. Pringle, E.G., R. Dirzo and D.M. Gordon. 2012. Plant defense, herbivory, and the growth of Cordia alliodora trees and their symbiotic Azteca ant colonies. Oecologia 170: 677–685. Postawa, T. and A. Furman. 2014. Abundance patterns of ectoparasites infesting different populations of Miniopterus species in their contact zone in Asia Minor. Acta Chiropt. 16: 387–395. Ratnasingham, S. and P.D.N. Hebert. 2013. A DNA-based registry for all animal species: the barcode index number (BIN) system. PLoS One 8: e66213. Reiczigel, J. and L. Rózsa. 2005. Quantitative Parasitology 3.0. Budapest. Distributed by the authors. Reisen, W.K., M.L. Kennedy and N.T. Reisen. 1976. Winter ecology of ectoparasites collected from hibernating Myotis velifer (Allen) in southwestern Oklahoma (Chiroptera: Vespertilionidae). J. Parasitol. 62: 628–635. Rivera-García, K.D., C.A. Sandoval-Ruiz, R.A. Saldaña-Vazquez and J.E. Schondube. 2016. The effect of seasonality on host-bat fly ecological networks in a temperate mountain cave. Parasitology 144: 692–697.

Rzedowski, J. 1981. Vegetación de México. Editorial Limusa, Mexico City. pp. 434. Sponchiado, J., G.L. Melo, G.A. Landulfo, F.C. Jacinavicius, D.M. Barros-Battesti and N.C. Cáceres. 2015. Interaction of ectoparasites (Mesostigmata, Phthiraptera and Siphonaptera) with small mammals in cerrado fragments, western Brazil. Exp. Appl. Acarol. 66: 369–381. Stanko, M., B.R. Krasnov and S. Morand. 2006. Relationship between host abundance and parasite distribution: inferring regulating mechanisms from census data. J. Anim. Ecol. 75: 575–583. Stoner, K.E., K.A.O. Salazar, R.C.R. Fernández and M. Quesada. 2003. Population dynamics, reproduction, and diet of the lesser long-nosed bat (Leptonycteris curasoae) in Jalisco, Mexico: implications for conservation. Biodivers. Conserv. 12: 357–373. Swofford, D.L. 2003. PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, MA. Tinsley, R.C., J.E. York, A.L.E. Everard, L.C. Stott, S.J. Chapple and M.C. Tinsley. 2011. Environmental constraints influencing survival of an African parasite in a north temperate habitat: effects of temperature on egg development. Parasitology 138: 1029–1038. Tlapaya-Romero, L., A. Horváth, S.Gallina-Tessaro, E.J. Naranjo and B. Gómez. 2015. Prevalencia y abundancia de moscas parásitas asociadas a una comunidad de murciélagos caverncolas en La Trinitaria, Chiapas, México. Revista Mexicana de Biodiversidad 86: 377–385. Valtonen, E.T., J.C.J. Holmes, J. Aronen and I. Rautelehti. 2003. Parasite communities as indicators of recovery from pollution: parasites of roach (Rutilus rutilus) and perch (Perca fluviatilis) in Central Finland. Parasitology 126: S43–S54. Villegas-Guzman, G.A., C. López-González and M. Vargas. 2005. Ectoparasites associated to two species of Corynorhinus (Chiroptera: Vespertilionidae) from the Guanaceví Mining Region, Durango, Mexico. J. Med. Entomol. 43: 125–127. Vink, C.J., P. Paquin and R.H. Cruickshank. 2012. Taxonomy and irreproducible biological science. BioScience 62: 451–452. Warburton, E.M., C.A. Pearl and M.J. Vonhof. 2016. Relationships between host body condition and immunocompetence, not host sex, best predict parasite burden in a bat-helminth system. Parasitol. Res. 115: 2155–2164. Wenzel, R.L. 1976. The streblid batflies of Venezuela (Diptera: Streblidae). Brigham Young University. Science Bulletin. Biological Series 2: 1–177. Wenzel, R.L., V.J. Tipton and A. Kiewlicz. 1966. The streblid ­batflies of Panama (Diptera: Calypterae: Streblidae), p. 405–675. In: (R.L. Wenzel and V.J. Tipton, eds.) Ectoparasites of Panama. Field Museum of Natural History, Chicago. pp. 861. Zahn, A. and D. Rupp. 2004. Ectoparasite load in European vespertilionid bats. J. Zool. 262: 383–391. Zarazúa-Carbajal, M., R.A. Saldaña-Vázquez, C.A. Sandoval-Ruiz, K.E. Stoner and J. Benitez-Malvido. 2016. The specificity of host-bat fly interaction networks across vegetation and seasonal variation. Parasitol. Res. 115: 4037–4044. Zhang, L., S. Parsons, P. Daszak, L. Wei, G. Zhu and S. Zhang. 2010. Variation in the abundance of ectoparasites mites of flatheaded bats. J. Mammal. 91: 136–143.

Authenticated | [email protected] author's copy Download Date | 2/27/18 1:24 AM

Suggest Documents